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Supergirl is the 17 year-old cousin of Superman and the last known Daughter of Krypton. Trapped in a meteor moments after escaping the destruction of the planet Krypton, Kara Zor-El finally managed to reach Earth only to discover her "baby cousin" had grown to become one of the planet's greatest heroes.

Adopting her cousin's symbol, Kara struggles to adapt to life on Earth; torn between the desire to live a normal life and the desire to uphold the heroic legacy of her cousin.

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When the Kryptonian scientist, Jor-El, attempted to warn the Science Council of the planet's impending destruction, while the council dismissed his assertions as paranoia, Jor-El's brother, Zor-El, heeded his brother's warnings and reverse-engineered force field technology left behind from when Brainiacbottled the city of Kandor. Although Zor-El could not perfect the device, he did succeed in creating a force field bubble that would enable Argo City to survive Krypton's destruction. However, Brainiac sensed that his technology was being used elsewhere and tracked Argo City down. He assimilated the city and merged it with the bottled city of Kandor as Krypton was in the process of exploding.
During the assimilation, Zor-El and his wife, Alura, sent their daughter, Kara Zor-El, in a rocket ship programmed to follow after that of baby Kal-El to Earth. While she was originally intended to look after her infant cousin upon their arrival, her rocket was caught in a meteor that sent her rocket off course and trapped her in stasis for decades.

When the meteor Kara's rocket was trapped within entered Earth's sector on a collision course with Earth, U.S. President Lex Luthor attempted to use the meteor, which was obviously of Kryptonian origin, in a campaign to make Superman a public fugitive. While Luthor issued a considerable bounty for the hero's capture, a bounty that numerous villains attempted to collect, and recruited a small taskforce of heroes, lead by Captain Atom, to apprehend him, the Batman aided the hero in fending of the bounty hunters and well-meaning apprehenders. As the meteor was destroyed by Captain Atom, Luthor attempted to kill Superman himself; publicly donning his LexCore battle armour to engage the hero in Metropolis only to be defeated and publicly outed as having formed an alliance with the New God, Darkseid for weapons and Apokoliptian technology.

While Luthor's presidency was revoked, the villain escaped and the meteor's destruction resulted in fragments of Kryptonite meteors being scattered across the planet. One such fragment contained Kara's rocket, which crashed into the Gotham City harbor. Awakening from stasis, Kara commandeered the Batboat when the Batman arrived to inspect the meteor and discovered the rocket. Exhibiting enhanced powers and strength, in an unfamiliar city unable to speak or understand the language, Kara inadvertently caused a trail of destruction through the city before being subdued by Batman after he deduced she was a kryptonian.
After alerting Superman, the two kryptonians converse and she tells him of their relationship as cousins. Ecstatic over the possibility of no longer being the last of his race, Superman takes Kara into his confidence, teaching her about life on Earth before Wonder Woman abducts her after receiving a prophesy that she would be abducted by Darkseid. Taking Kara to Themyscira, Diana begins training her in combat despite Superman's rejections, however, Kara is still abducted while the "Trinity" (Batman, Superman, Wonder Woman) and Amazons are distracted by an army of Doomsday clones.

Supergirl, located in the Meta Wing of the JLA Watchtower, will initiate the Level 30 mission to locate and assist her cousin, Superman, who is currently inside the Daily Planet building that is being shrunk and bottled by Brainiac.

Supergirl is called upon by the Justice League to investigate reports of metahuman experimentation in a LexCorp-funded wing of Metropolis General Hospital. She finds extensive evidence of metahuman experimentation conducted by Dr. Psycho and attempts to liberate the meta-humans. She is thwarted and her DNA sampled by one of the new metahumans supported by the Secret Society of Super-Villains working for Lex Luthor.

Supergirl is an iconic opponent for villains in Alternate Metropolis in the Brothers in Arms operation.

To celebrate the premier of the CBS Supergirl television series on October 26th, 2015, DC Universe Online temporarily updated Supergirl's in-game look to match her television appearance. This updation was initiated on the 22nd of October, 2015, a month after which she returned to her typical in-game look. Her "television series" appearance is now available as a Legends PvP avatar.